Genome duplication in amphibians and fish: an extended synthesis

Abstract

Whole genome duplication (leading to polyploidy) is widely accepted as an important evolutionary force in plants, but it is less recognized as a driver of animal diversification. Nevertheless, it occurs across a wide range of animals; this review investigates why it is particularly common in fish and amphibians, while rare among other vertebrates. We review the current geographic, ecological and phylogenetic distributions of sexually reproducing polyploid taxa before focusing more specifically on what factors drive polyploid formation and establishment. In summary, (1) polyploidy is phylogenetically restricted in both amphibians and fishes, although entire fish, but not amphibian, lineages are derived from polyploid ancestors. (2) Although mechanisms such as polyspermy are feasible, polyploid formation appears to occur principally through unreduced gamete formation, which can be experimentally induced by temperature or pressure shock in both groups. (3) External reproduction and fertilization in primarily temperate freshwater environments potentially exposes zygotes to temperature stress, which can promote increased production of unreduced gametes. (4) Large numbers of gametes and group breeding in relatively confined areas could increase the probability of compatible gamete combinations in both groups. (5) Both fish and amphibians have a propensity to form reproductively successful hybrids; although the relative frequency of autopolyploidy versus allopolyploidy is difficult to ascertain, multiple origins involving hybridization have been confirmed for a number of species in both groups. (6) Problems with establishment of polyploid lineages associated with minority cytotype exclusion could be overcome in amphibians via assortative mating by acoustic recognition of the same ploidy level, but less attention has been given to chemical or acoustic mechanisms that might operate in fish. (7) There is no strong evidence that polyploid fish or amphibians currently exist in more extreme environments than their diploid progenitors or have broader ecological ranges. (8) Although pathogens could play a role in the relative fitness of polyploid species, particularly given duplication of genes involved in immunity, this remains an understudied field in both fish and amphibians. (9) As in plants, many duplicate copies of genes are retained for long periods of time, indicative of selective maintenance of the duplicate copies, but we find no physiological or other reasons that could explain an advantage for allelic or genetic complexity. (10) Extant polyploid species do not appear to be more or less prone to extinction than related diploids in either group. We conclude that, while polyploid fish and amphibians share a number of attributes facilitating polyploidy, clear drivers of genome duplication do not emerge from the comparison. The lack of a clear association of sexually reproducing polyploids with range expansion, harsh environments, or risk of extinction could suggest that stronger correlations in plants may be driven by s...

Can resource costs of polyploidy provide an advantage to sex?

“…Since ploidy-level variation can affect traits from gene expression to the rate of spread of beneficial mutations to immune function (reviewed in Otto and Whitton, 2000;Comai, 2005;Mable et al, 2011;King et al, 2012), it may be of relevance when considering the outcome of competition between sexual and asexual lineages that differ in ploidy.…”

“…The advantages and disadvantages of polyploidy and its relevance to the distribution and maintenance of sex have been reviewed extensively (Bierzychudek, 1985 The ecological consequences of polyploidy are difficult to empirically disentangle from those directly related to asexuality, with which it is so often associated (Bierzychudek, 1985;Otto and Whitton, 2000;Hörandl, 2006;Mable et al, 2011). In a diverse array of plants and animals, asexual lineages (Vandel, 1940;Suomalainen, 1950;Ghiselin, 1974;Levin, 1975;Bell, 1982;Lynch, 1984;Law and Crespi, 2002;Hörandl, 2006) and polyploid taxa (Vandel, 1928;Bierzychudek, 1985;Beaton and Hebert, 1988;Kearney, 2005;Maniatsi et al, 2011) increase in abundance at higher latitudes or altitudes relative to their sexual and/or lower ploidy counterparts.…”

Efficient screening for ‘genetic pollution’ in an anthropogenic crested newt hybrid zone

“…Although polyploidy and paralogy could underlie this pattern we consider this unlikely because: (1) polyploids are rare in salamanders and have virtually never been recorded in Triturus newts (Borkin et al 1996;Litvinchuk et al 2001;Mable et al 2011), (2) the initial marker design phase excluded multicopy genes (Wielstra et al 2014), and (3) the distribution of unclear SNP calls was not linked to any particular individuals or markers. An alternative explanation is that ambiguous SNP calls are a consequence of the large genome size of our study system (c. 20-30 Gb in the genus Triturus; Gregory 2016).…”

Genetic mapping in polyploids

“…However examples do exist, particularly in amphibians and fish (but much less so in other vertebrates) (Mable et al, 2011). Amphibious examples include the BluespottedJefferson salamander complex (Uzzell, 1964), the grey tree-frog Hyla versicolor (Ptacek et al, 1994), the American ground frog Odontophrynus americanus (Beçak et al, 1966) and the African clawed frog Xenopus laevis (Session et al, 2016).…”